Patterns of putative gene loss suggest rampant developmental system drift in nematodes

Abstract

Gene loss often contributes to the evolution of adaptive traits. Conversely, null mutations frequently reveal no obvious phenotypic consequences. How pervasive is gene loss, what kinds of genes are dispensable, and what are the consequences of gene loss? The nematode Caenorhabditis elegans has long been at the forefront of genetic research, yet only recently have genomic resources become available to situate this species in its comparative phylogenetic and evolutionary context. Here, patterns of gene loss within Caenorhabditis are evaluated using 28 nematode genomes (most of them sequenced only in the past few years). Orthologous genes detected in every species except one were defined as being lost within that species. Putative functional roles of lost genes were determined using phenotypic information from C. elegans WormBase ontology terms as well as using existing C. elegans transcriptomic datasets. All species have lost multiple genes in a species-specific manner, with a genus-wide average of several dozen genes per species. Counterintuitively, nearly all species have lost genes that perform essential functions in C. elegans (an average of one third of the genes lost within a species). Retained genes reveal no differences from lost genes in C. elegans transcriptional abundance across all developmental stages when considering all 28 Caenorhabitis genomes. However, when considering only genomes in the subgeneric Elegans group, lost genes tend to have lower expression than retained genes. Taken together, these results suggest that the genetics of developmental processes are evolving rapidly despite a highly conserved adult morphology and cell lineage in this group, a phenomenon known as developmental system drift. These patterns highlight the importance of the comparative approach in interpreting findings in model systems genetics.